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Comprehensive Gene Expression Profiling of Peyer’s Patch M Cells, Villous M-Like Cells, and Intestinal Epithelial Cells¹

Kazutaka Terahara^2,*,, Masato Yoshida^2,*,, Osamu Igarashi^*,, Tomonori Nochi^*,, Gemilson Soares Pontes^*, Koji Hase, Hiroshi Ohno, Shiho Kurokawa^*, Mio Mejima^*, Naoko Takayama^*,, Yoshikazu Yuki^*,, Anson W. Lowe^¶ and Hiroshi Kiyono^3,*,,

^* Division of Mucosal Immunology, Department of Microbiology and Immunology, The Institute of Medical Science and Department of Medical Genome Science, Graduate School of Frontier Science, The University of Tokyo, Tokyo, Core Research for Evolutional Science and Technology, Japan Science and Technology Corporation, Saitama, and Laboratory of Epithelial Immunobiology, Research Center for Allergy and Immunology, Institute of Physical and Chemical Research, Yokohama, Japan; and ^¶ Department of Medicine, Stanford University, Stanford, CA 94305

Separate populations of M cells have been detected in the follicle-associated epithelium of Peyer’s patches (PPs) and the villous epithelium of the small intestine, but the traits shared by or distinguishing the two populations have not been characterized. Our separate study has demonstrated that a potent mucosal modulator cholera toxin (CT) can induce lectin Ulex europaeus agglutinin-1 and our newly developed M cell-specific mAb NKM 16-2-4-positive M-like cells in the duodenal villous epithelium. In this study, we determined the gene expression of PP M cells, CT-induced villous M-like cells, and intestinal epithelial cells isolated by a novel approach using FACS. Additional mRNA and protein analyses confirmed the specific expression of glycoprotein 2 and myristoylated alanine-rich C kinase substrate (MARCKS)-like protein by PP M cells but not CT-induced villous M-like cells. Comprehensive gene profiling also suggested that CT-induced villous M-like cells share traits of both PP M cells and intestinal epithelial cells, a finding that is supported by their unique expression of specific chemokines. The genome-wide assessment of gene expression facilitates discovery of M cell-specific molecules and enhances the molecular understanding of M cell immunobiology.

The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked advertisement in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

¹ This work was supported in part by grants from Core Research for Evolutional Science and Technology of the Japan Science and Technology Corporation, the Ministry of Education, Science, Sports, and Culture, and the Ministry of Health and Welfare in Japan.

² K.T. and M.Y. contributed equally to this work and share first authorship.

³ Address correspondence and reprint requests to Dr. Hiroshi Kiyono, Division of Mucosal Immunology, Department of Microbiology and Immunology, The Institute of Medical Science, The University of Tokyo, 4-6-1 Shirokanedai, Minato-ku, Tokyo 108-8639, Japan. E-mail address: kiyono{at}ims.u-tokyo.ac.jp

⁴ Abbreviations used in this paper: FAE, follicle-associated epithelium; 7-AAD, 7-amino actinomycin; CKLF, chemokine-like factor; CT, cholera toxin; DAPI, 4'-6-diamidino-2-phenylindole; IEC, intestinal epithelial cell; IEL, intraepithelial lymphocyte; ISH, in situ hybridization; MLP, myristoylated alanine-rich C kinase substrate (MARCKS)-like protein; PP, Peyer’s patch; UEA-1, Ulex europaeus agglutinin-1; WGA, wheat germ agglutinin.

⁵ The online version of this article contains supplemental material.

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